1975), is ofwe have failed in severa respects: 1.. We have ignored interesting biological problems and questions. 2. We have not been particularly interested in the consequences of
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Introduction
Interindividual variability: an underutilized resource
AL
BE
RT
F.
BE
NN
ET
T
Two principal analytical approaches have been used in studies of organism
al physiology. T
hese are represented by the terms "com
parative physiology" and "physiological ecology." T
he form
er compares functional characters in
two or m
ore populations, species, or higher taxa in an attem
pt to understand m
echanism.
Biological diversity is used to
help understand principles of
physiological design. Often the experim
ental species are chosen specifically because their system
s demonstrate an extrem
e phenomenon o
r because the experim
ental preparation is technically accessible. Th
e selection of a species on
these grounds is known as the K
rogh Principle (Krogh, 1929; K
rebs, 1975), w
hich has been very influential and successful in guiding studies in com
parative physiology for more than fifty years.
The second approach, physiological
ecology or ecological physiology,
examines the physiological attributes of a species and interprets them
in the context of the natural environm
ent or ecological niche of an animal. T
hese studies concentrate on analysis of adaptive pattern, of how
physiology, mor-
phology, and behavior interact to permit survival and reproduction in a given
environment. In this approach, em
phasis is placed on ecological and evolu- tionary aspects of physiological function. M
onitoring the organism in its
natural environment and speculation on selective factors that influenced the
evolution of
characters are the principal
interpretive contexts of
these studies.
These tw
o approaches are by no m
eans exclusive and have often proved com
plementary. T
hey have yielded a substantial understanding of how ani-
mals w
ork and function in the natural world. H
owever, m
y thesis here is that both approaches have overlooked a valuable source of inform
ation. In their concentration on population-, species-, or higher-level phenom
ena, [hey have failed to
analyze and take advantage of biological
differences am
ong individuals. As traditionally practiced, physiological studies neglect
differences among individual anim
als and attempt to
describe the functional response in the average anim
al of the group. I believe that this approach has been very short-sighted and that the study of interindividual differences has
147
much to contribute to both com
parative physiology and physiological ecol- ogy. I w
ill argue that the analysis of the bases and consequences of interin- dividual variability can provide new
tools for both types of physiological
analysis. I believe that it is also capable of building
new and im
portant bridges to other allied fields of biology, especially ecology, ethology, evolu- tion, and genetics.
Th
e tyrann
y of the Go
lden
Mean
Th
e framew
ork of physiological studies implicitly em
phasizes the descrip- tion and analysis of central tendency. D
epending on the data, this involves the calculation of m
ean values or the development of least-squares regression
equations. After these values are determ
ined, they take on a life of their own
and become the only
point of
analysis and com
parison. Th
e complete
breadth of biological variation determined in the investigation then is for-
gotten. Measures of variability (e.g., variance, standard deviation) are calcu-
lated and reported only to stipulate confidence limits about the m
ean or slope of the regression line. G
roups are then compared to determ
ine whether they
are different from one another o
r from hypothesized values. T
he variability inherent in the original data is seen only as "noise,"
through which the
"true" value of the central tendency can be glimpsed w
ith appropriate statis- tical techniques.
This assum
ption of a "true" or "real"
central tendency, which biological
reality only approxim
ates, stems from
P
latonic philosophical
traditions. T
hese maintain that ideal archetypes exist that can be perceived only im
per- fectly through perceptual sensation. T
he concept of an ideal form of a struc-
ture or process w
as central to the thinking of medical physiologists of post-
Renaissance E
urope and heavily influenced the functional biologists of the nineteenth century. T
hese physiologists and morphologists, in their search
for proximate causation, m
aintained a typological approach to experimen-
tation and analysis and were largely unaffected by contem
poraneous devel- opm
ents in evolutionary biology and genetics (cf. Mayr, 1982, for a m
ore detailed discussion). A
nalysis of variability played an important role in these
latter fields, but it w
as ignored by functional biologists at the tim
e and rem
ains largely unexplored by them even today.
To
dispel any doubt that analysis of central tendency and neglect of vari- ability is the dom
inant or exclusive analytical m
ode in organismal physiol-
ogy, I reviewed all papers published during 1985 in the Journal of C
ompar-
ative Physiology, the Journal of E
xperimental B
iology, and Physiological Z
oology. These are som
e of the best and most forw
ard-looking journals in the field. N
early all the articles reported mean values or regression equations
and did statistical analyses. H
owever, less than
5%
of the articles even
reported the range of values of the data obtained, and out of more than 250
BUR
ST SPEED (crnls)
DISTAN
CE C
RAW
LED (m
)
FIG
UR
E 7.1
Frequency distributions of burst speed and total distance craw
led under pursuit by individual newborn garter snakes (T
hamno-
phis radix). Each individual observation is the mean of tw
o trials con- ducted on tw
o successive days; individual repeatability is highly signif- icant (r =
0.60 for burst speed and 0.55 for distance; p < .001).
Distance craw
led is reported on a logarithmic axis. (D
ata from A
rnold and B
ennett, in press.)
articles, only one (Taigen and W
ells, 1985) analytically examined the varia-
bility in the observations. T
he concentration on central tendency has been and will continue to be
very useful in testing certain hypotheses, but it has distracted us from an
examination of
the causes and consequences of biological variability. An
example of this variability is given in Figure 7.1, in this case variability in
locomotor perform
ance capacity of newborn garter snakes. M
aximal burst
speed and the total distance crawled under pursuit w
ere measured in nearly
150 laboratory-born animals shortly after birth (A
rnold and Bennett,
in press). T
hese behaviors are individually repeatable (see below) and represent
the breadth of response of the population at birth, before natural selection by the external environm
ent has had the opportunity to act. B
oth these per- form
ance measures show
strong central tendencies, but they also show enor-
mous interindividual variability. T
he fastest snake has a burst speed ten times
that of the slowest; the endurance of som
e individuals is more than tw
enty tim
es that of others. Assum
ing for a mom
ent that these individual differences are real (see below
), these observations imm
ediately suggest two sorts of ques-
tions. First, what is the functional basis of these individual perform
ance dif- ferences? W
hich physiological or m
orphological factors make a fast snake
fast and which account for the relatively low
stamina of som
e other animals?
Second, w
hat are the ecological and evolutionary consequences of these dif- ferences? Is there differential survivorship or grow
th under natural condi- tions based on locom
otor performance capacities? T
hese questions reflect the som
ewhat artificial dichotom
y raised earlier between com
parative physiol- ogy and physiological ecology, but both o
f them reflect com
pelling questions of general biological interest. T
hey are obscured, however, if one concen-
trates only on central tendency. This is the tyranny of the G
olden Mean: it
restricts our vision of the data and narrows our conceptual fram
ework so
that we cannot take advantage of all the analytical possibilities of biologica
variability. T
he failure to consider interindividual variability is not that of ecologica
or comparative physiology alone. A
lmost identical com
ments and com
pari sons could be m
ade about any other field of organismal biology.
In our concentration
on central
tendency, w
e have
failed in
severa respects:
1.. We have ignored interesting biological problem
s and questions. 2. W
e have not been particularly interested in the consequences of the dati w
e have gathered for survivorship or fitness. 3. W
e have failed to utilize the breadth of our data in assessm
ent of physio logical hypotheses.
4. We have failed to provide sufficient inform
ation in our research report that w
ould permit others to
analyze biological variability.
The reality o
f interindividual variability
I believe rhat part of the difficulty rhat most ecological and com
parative phys iologists have in reporting and utilizing variability is a suspicion of its realit] and inform
ation content. Biological m
easurements are inherently highly var
iable as compared to those m
ade by physicists or chemists. C
oefficients o variation of 20 to 30%
, values that would cause a physical scientist to blanch
are routine in most physiological m
easurements. T
o w
hat extent, however
is this variability real and useful? It seems to m
e that there are three potentia objections to its use:
I. Extrem
e values are atypical or abnorm
al and do
not reflect the trut response of m
ost individuals.
This view
is essentially a restatement of the typological concept: the aver
age is the real. Extrem
e performance certainly is "atypical"
and "abnormal'
in the strict sense of the words, but that does not m
ean that it is not real. A physiologist m
ust be sure that experimental anim
als are in good condition, but it shouId go w
ithout saying that one must have external cause to doubt
any data point. It cannot be questioned only because it happens to lie on the extrem
e of the range.
This view
suggests that the experimenter has m
ore confidence in values that lie closer to
the mean than those at the extrem
es. If this is the case, then not all points should receive equal w
eighting: those closer to the m
ean should be w
eighted more highly. T
he circularity of this logic is apparent. F
urther, norm
al parametric statistics are inappropriate in such a circum
stance. Either
all data points receive equal confidence and equal weight, o
r the analytical m
ethods we norm
ally use are inapplicable; one cannot have it both ways.
2. Observed variability
is due to instrum
entation or procedural error; the
observed range does not result from real biological differences but from
inaccuracies in experim
ental setups or procedures.
According to
the type of m
easurement, this objeccion
may
have some
validity. How
ever, the precision of modern physiological equipm
ent is typi- cally less than
1% and is consequently a doubtful explanation of
much
higher apparent biological variability. Further, if such errors are felt to
be im
portant, their magnitude m
ust be quantified and analyzed (although they alm
ost never are) even in studies that are interested only in central tendency. If the errors are random
, then the mean values w
ill be correct, but the mea-
surements of variance and standard deviation of the m
eans will be inflated.
As statistical com
parisons between groups are dependent on the extent of
intragroup variability, incorrect judgments m
ay be made if experim
ental or
instrumentation error is not analyzed and rem
oved. Consequently, if this type
of error is a problem, it is not a special problem
in the'analysis of variability alone. It also affects any kind of analysis, including that of central tendency.
3. The variation
measured is
real but reflects random
and
unrepeatable responses of individuals;
that is, intraindividual variability is so high that there is n
o significant interindividual com
ponent to total variance.
This is by far the m
ost serious potential objeccion to the analysis of vari-
ability: if the responses are random w
ith respect to individuals, then analyz-
ing the differences among individuals is futile. T
he m
easurements required
to demonstrate w
hether this is an important problem
are a series of repeated observations on the sam
e individuals and analysis of the significance of the individual com
ponent. For instance, if one is interested in oxygen transport
capacity, one might m
easure maxim
al oxygen consumption in each of several
individuals on
sequential days to determ
ine whether som
e individuals have consistently high o
r low capacities.
Given the general lack of interest in interindividual variability, analyses of
intra- versus interindividual variability are relatively few
in ecological or
comparative physiological studies. M
ost of these relate to data on locom
otor perform
ance capacity, and many of the exam
ples in this discussion will be
drawn from
this area. Individual locomotor perform
ance ability has a sig- nificant repeatable interindividual com
ponent in every study in which it has
15
2
AL
BE
KT
F
. B
EN
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TT
TABLE 7.1 Studies dem
onstrating significant interindividual variability in locom
otor performance
- -
Gro
up
P
erformance
No
. of species
Lizards burst speed
6" 1 2c
2d
1'
stamina
6" 1' ld
defensive b
eh
avio
r 1"
Snakes
burst speed In 1
stamina
1
defensive behavior 1
' A
nurans stam
ina 2'
"ennett (1 980).
bC
row
ley and P
ietruszka (19
83
). 'H
ue
y an
d H
ertz (1 98
4).
dGarland (1 984, 1985).
'Crow
ley (1 985).
'Joh
n-A
lde
r (1 984). G
arla
nd
and Arn
old
(1983). h
~rn
old
and B
ennett (in press).
'Arn
old
an
d B
en
ne
tt (1984). 'P
utnam and B
ennett (1981).
been examined (T
able 7.1). An exam
ple of individual constancy of day-to-day differences in locom
otor performance is given in Figure 7.2 (B
ennett, 1980). M
aximal burst speed w
as measured in fifteen adult fence lizards on five
sequential days. Rank order of perform
ance was conserved through the re-
petitive trials (p < .001). T
hese individual differences in burst speed capacity w
ere independent of both sex and body mass, Sim
ilarly, individual perfor m
ance rank is stable even when the internal environm
ent of the animals is
grossly altered, as during changes in body temperature. Individual rankings
of burst speed performance of alligator lizards at different body tem
peratures are given in T
able 7.2. Again, individual differences are highly significant (P
< .O
OI): som
e animals are fast and som
e are slow at all body tem
peratures (see also H
uey and Hertz, 1984).
I believe that locomotor m
easurements w
ould a priori be among the least
repeatable of any of the potential spectrum of "physiological"
measurem
ents. T
hey may be influenced by a great m
any motivational and psychological fac-
tors, as well as differences in underlying physiological
or m
orphological
Fl G U
RE
7.2 R
ank order performance of burst speed in fifteen adult
fence lizards (Sceloporus occidentalis) measured on five successive
days. Rank 1 is the fastest anim
al, rank 15
is the slowest. D
ots indicate rank perform
ance on each day; vertical bars, range; horizontal bars, m
ean rank. Individual ranking effects are highly significant (p < .001
by Kendall's coefficient of concordance). (D
ata from B
ennett, 1980,
and unpublished observations.)
capacity. From
that viewpoint, a significant interindividual com
ponent in m
easurements of locom
otor capacity might suggest that m
any other physi- ological variables w
ould also have individual fidelity. Significant interindividual
differences have been
demonstrated in such
diverse systems and m
easures as maxim
al oxygen consumption in am
phibi- ans and lizards (P
ough and Andrew
s, 1984; Wells and T
aigen, 1984; Sullivan and W
alsberg, 19853, enzymatic activities in fruit flies (L
aurie-Ahlberg et al.,
1980), cuticular water loss in cicadas (T
oolson, 19841, muscular m
orphology of birds (B
erman, C
ibischino, Dellaripa, and M
ontren, 19851, skeletal mor-
phology of salamanders (H
anken, 19831, kinematics and m
uscle activity pat- terns during feeding in salam
anders (Shaffer and Lauder, 1985a, 1985b), for-
aging tactics in fish (R
ingler, 1983), food preferences in snakes (Arnold,
1981), and regulated body temperatures of lizards (C
hristian, Tracy, and Por-
ter, 1985).
15
4
AL
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. B
EN
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TT
TA
BL
E 7.2 R
ank order of burst speed at different body temperatures in tw
elve individual alligator lizards (C
errhonotus multicarinatus)
Ind
ividu
al
Tem
perature ("a
A
B C
DE
F
GH
I
1 K
L
10
8
7 3
11
4
9.5 1
9.5 2
5 1
2
6 1
5
85
11
13
6
21
07
91
24
2
0
7 6
2 11
3 8.5
5 8.5
1 4
12 10
2 5 9
82
11
3
4 6
7 1
12
1
05
3
0
6 9
2 1
2
7.5 5
4 1
0
1 7.5
11
3
35
8
10
7
11
5.5
2 4
9 1
5.5 1
2
3 37.5
9 8
7 1
1
6 3.5
1 1
0
2 3.5
12 5
Note: R
ank 1 = fastest; p <
,001 by Kendall's coefficient o
f concordance. S
ource: Bennett (1 980).
In my opinion, the large m
ajority of physiological variables that can be sam
pled repeatedly will show
real and significant interindividual variation. T
he question then becom
es how w
e can utilize this variability to our benefit
in asking analytical questions.
Th
e analytical u
tility of in
terind
ividu
al variation
I suggest four different types of studies in which the exploration of interin-
dividual variability might play a crucial role. Som
e represent new sorts of
investigations for ecological or com
parative physiology. Others perm
it a new
approach to both current and classical questions in the fields.
The testing of correlative hypotheses
A com
mon analytical approach in com
parative physiology is to m
easure the correlation betw
een two
or m
ore variables in two o
r more groups (e.g., pop-
ulations, species) and to infer mechanistic relationships if significant corre-
lations exist. For example, if positive associations are found betw
een the length of the loops of H
enle in kidneys of various mam
mals and their ability
to concentrate urine,. one m
ight conclude that these may be functionally
linked. These correlational exam
inations have been central in building the field of com
parative physiology. They have, how
ever, been criticized for their failure to
take into account the phylogenetic history of the experimental ani-
mals involved (G
ould and Lew
ontin, 1979; Felsenstein, 1985; Chapter 4).
A com
panion approach to interspecific analyses is the exam
ination of interindividual correlations of
variables w
ithin a species. This approach
maintains the benefits of com
parative analysis without som
e of the objections associated w
ith using organisms that are distantly related phylogenetically
(see Chapter 4). If tw
o factors are functionally related, they should be signif- icantly correlated am
ong individuals within a species. In fact, if evolutionary
or functional trends are proposed, the argument is strengthened if intraspe-
cific associations can be demonstrated, because selection on traits w
ithin populations m
ust be the ultimate source of adaptation.
The experim
ental protocol required to investigate interindividual variabil- ity is sim
ilar to that of interspecific comparative studies, except that obser-
vations on functional traits of interest must be m
ade on the same individuals
and analyzed on that basis. The researcher then correlates one trait w
ith the other to determ
ine whether they are positively o
r negatively associated. If so, the hypothesis of functional relationships am
ong the traits is supported, and further experim
entation can be planned to explore the nature of the rela-
tionship (see Huey and B
ennett, 1986). If no
significant association is found, then the traits are not functionally linked and the hypothesis is rejected.
One im
portant step in this analysis is the determination of the dependence
of the traits in question on body size (mass) and the elim
ination of such a dependence in the analysis.
So many m
orphological, physiological, and
behavioral traits are dependent on body size (see Calder, 1984; Schm
idt-Niel-
sen, 1984) that it is very easy to obtain positive correlations among otherw
ise unrelated traits because of their m
utual dependence on mass (see A
ppendix for a further discussion and exam
ple). Allom
etric analyses should be per- form
ed (see Chapter 10) and, if m
ass effects are significant, the mass-corrected
residuals'should be analyzed for correlation. A
n illustrative example of the use of interindividual variability in testing
correlative hypotheses may be beneficial here. T
hese data are drawn from
som
e observations on the skeletal muscle physiology and locom
otor perfor- m
ance of tiger salamanders (E
lse and Bennett, 1987, and unpublished obser-
vations). Close (1964,1965) proposed a correlation betw
een the speed of iso- m
etric and isotonic contractions of skeletal muscle: the m
aximal velocity of
shortening (isotonic) is supposed to be positively related to
the rate of tension developm
ent in an isometric tw
itch or tetanus. T
his proposal is a straight- forw
ard mechanistic linkage that is supported by interspecific com
parative studies. W
e can test this hypothetical connection by making observations of
all these factors on individual animals and determ
ining whether they are
associated within individuals. A
further correlation that might also be inves-
tigated is the association between m
uscle contractile speed and locomotor
speed: are the animals that have the greatest intrinsic speed of m
uscle con- traction also the fastest? First, all variables are m
ass-corrected and the resid- uals are then correlated w
ith each other in Table 7.3. C
orrelations are sig- nificant am
ong isometric variables and betw
een isotonic variables, but no associations are significant betw
een any isotonic and isometric variable nor
- betw
een burst speed and any measure of m
uscle contractile performance.
TA
BL
E 7.3
Co
rrela
tion
coe
fficien
ts (r) am
on
g m
ass-co
rrecte
d re
sidu
als o
f loc
om
oto
r pe
rform
an
ce
an
d m
uscle
con
tractile
fa
ctors in
the
sala
ma
nd
er A
mb
ystom
a tig
rinu
rn n
eb
ulo
sum
at 20
"C (n
= 20)
Isometric m
uscle factors Isotonic m
uscle factors
Locomotion
Tetanic
Tw
itch
Maxim
al M
aximal
(burst swim
T
etanic T
witch
contraction
contraction rate o
f pow
er speed)
force force
rate rate
shortening output
Burst ru
n speed
.13 -
Burst sw
im speed
Tetanic force
Tw
itch force
Tetanic contraction
rate T
witch
con
tractio
n
rate M
axim
al rate o
f .71*
shortening
Note: A
sterisks indicate significant correlations (r > 0.56, p
4 0.01).
Source: U
np
ub
lishe
d data of A
. F. Bennett, P
. L. Else, and T. G
arland.
INT
ER
IND
IVID
UA
L V
AR
IAB
ILIT
Y
15
7
These results argue against any necessary m
echanistic association among
these factors. T
his is only one example of an approach that can be utilized in m
any dif- ferent physiological o
r functional studies. For instance, the role of m
aximal
heart rate in limiting m
aximal oxygen consum
ption or that of a particular
muscle in generating force during feeding o
r locomotion could be investi-
gated using an appropriate analysis of interindividual variability.
Exam
ining the functional bases of organismal or physiological variables
Another use that can be m
ade of interindividual variability is the determi-
nation of which of a potential suite of characters m
ight influence perfor- m
ance at a higher level of biological organization. This is a m
ultivariate sta- tistical approach based
on an array of characters m
easured in
identified individuals of a species. T
he researcher measures a perform
ance variable, such as burst speed o
r lower critical tem
perature, and a number of m
orpho- logical an
d/o
r physiological predictor variables that might reasonably be
associated with it (e.g., lim
b length and maxim
al velocity of muscle short-
ening, or fur density and body tem
perature, respectively). All these m
easure- m
ents are made on the sam
e series of individuals. Mass dependence of any
of the factors is analyzed and removed, as discussed previously. T
hen step- w
ise multiple regression analysis (or another appropriate technique, such as
canonical correlation) is used to determine w
hich, if any, of the predictor variables are associated w
ith the performance variables.
An exam
ple of this approach is provided by the study of Garland (1984)
on locomotor perform
ance by a lizard, Ctenosaura sim
ilis. Endurance, burst
speed, and maxim
al distance run under pursuit were m
easured in a series of individuals, along w
ith a variety of physiological and morphological vari-
ables, including body mass and length; standard and m
aximal rates of oxygen
consumption and carbon dioxide production; m
ass of thigh muscle, heart,
and liver; hematocrit and hem
oglobin concentration of the blood; myofibril-
lar AT
Pase activity of thigh m
uscle; and activities of three selected metabolic
enzymes in heart, liver, and skeletal m
uscle tissue. Body m
ass effects were
removed by regressing all variables o
n m
ass and analyzing only mass-cor-
rected residuals. Each m
easure of locomotor perform
ance was then regressed
as a dependent variable on the suite of morphological and physiological char-
acters as independent variables. Th
e results of these analyses are given in T
able 7.4. N
early 90% of the m
ass-corrected interindividual variation in endurance could be attributed to
four predictive factors, including maxim
al oxygen consum
ption, skeletal muscle and heart m
ass, and hepatic aerobic enzym
e activity. This is a rem
arkable amount of predictive pow
er. More than
half the variation in maxim
al distance run is correlated with m
aximal carbon
dioxide production and anaerobic enzyme activity of the skeletal m
uscle. N
one of the variables measured in this study w
as significantly associated with
15
8
AL
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. B
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TA
BL
E 7.4 Stepw
ise multiple regression analysis of locom
otor performance of
the lizard Ctenosaura sim
ilis
Perform
ance V
ariable P
artial R2
Endurance
Th
igh
muscle m
ass 0.540
Ma
xima
l oxygen consumption
0.187 H
ea
rl mass
0.0
86
Liver aerobic enzym
e ac
tiv~
~y
O
.OUO
Total
0.893 (p
< .0001)
Distance ru
n
Ma
xima
l carbon dio
xide
pro
du
ction
0.405
Thigh anaerobic enzym
e activity 0.1 77
Total
0.582 (p
= .0022)
Burst speed
No
ne
N
.5.
Source: G
arland (1 984).
burst speed. Thus, a m
ultivariate statistical approach does not necessarily find a significant association am
ong any set of variables. It may uncover strong
correlations (as in the case of endurance) or no correlation (as with burst
speed). A subsequent investigation on another species of lizard found signif-
icant interindividual correlations between burst speed and glycolytic enzy-
matic activity of skeletal m
uscle and an inverse relationship between burst
speed and muscle fiber diam
eter (T. G
leeson, unpublished data). A
m
ultivariate statistical approach can be
particularly powerful w
hen num
erous underlying variables might be expected to
influence higher-level perform
ance. It can help to single out the most significant factors from
an entire array and allow
a researcher to concentrate further on those. T
he result of the analysis m
ay serve to confirm a priori associations or m
ay sug- gest entirely unexpected linkages that can be explored further. T
his multi-
variate analysis should be regarded as a first-stage approach, to be followed
by more detailed com
parative and experimental research o
n the factors iden-
tified with this technique. T
hese further studies hay
also take advantage of interindividual variability.
Measurem
ent of selective importance of traits under field or
experimental conditions
Physiological ecologists and comparative physiologists usually assum
e that the traits that they study are of
adaptive significance, that is, that they enhance survivorship and reproductive potential. T
his assumption is, how
- ever, alm
ost never tested directly (Arnold, 1983; E
ndler, 1986). Using inter-
individual variability, one can evaluate whether perform
ance of any given
physiological or organism
al trait is in fact correlated with differential sur-
vivorship under natural conditions. Th
e observations required involve scor- ing a trait on a large num
ber of individual animals, releasing them
into their natural environm
ent, and recapturing the survivors after exposure to this
environment. T
he survivors are then exam
ined to determ
ine whether they
are drawn from
any subset of the original distribution. Selection m
ight operate in a number of w
ays to favor different portions of the original distribution of the trait (Sim
pson, 1953; Lande and A
rnold, 1983; E
ndler, 1986). It might be directional and favor individuals at one end of the
range of variability. For example, d
o birds w
ith greater insulation survive better during the w
inter or do caterpillars that eat m
ore metam
orphose more
rapidly and successfully? Do
newborn snakes that are very fast or have a high
endurance (see Figure 7.1) accrue an advantage under natural conditions such that they are m
ore likely to survive to reproductive age? Selection m
ay also be stabilizing, favoring anim
als with m
odal values for a given trait, thereby reducing variability and reinforcing central tendency in the population. In these cases, both very w
ell and poorly insulated birds, caterpillars with both
large and small appetites, and very fast and very slow
snakes would be
selected against. Selection might also be disruptive, favoring anim
als at both extrem
es of the distribution and tending to increase overall variability. T
he
null hypothesis against which the presence of selection m
ust be tested is the absence of any detectable effect of the variable on such indices of fitness as survivorship, grow
th, or reproduction. In the exam
ples above, variability in plum
age quality, feeding capacity, or speed would have no detectable influ-
ence on fitness under field conditions. T
his correspondence betw
een physiological or perform
ance characters
and survivorship or fitness under field conditions is termed the "fitness gra-
dient" (Arnold, 1983). Its determ
ination is judged to be essential for the char- acterization of the ecological and evolutionary im
plications of any physio- logical variable. H
owever, com
prehensive studies of the fitness gradient have rarely been attem
pted for any variable. The effects of natural selection on
physiological variation generally are unknown (E
ndler, 1986). A lack of cor-
respondence between m
aximal oxygen consum
ption and some m
easures of reproductive perform
ance has been reported in adult male toads (W
ells and T
aigen, 1984; Sullivan and Walsberg, 1985), but its effect on differential sur-
vivorship up to adulthood has not been measured. Studies on the effects of
locomotor perform
ance on postnatal survivorship are currently underway on
fence lizards (R. H
uey, University of W
ashington) and garter snakes (my lab-
oratory). Th
e direct measurem
ent of the impact of a character on perfor-
mance under natural conditions, in spite of its obvious im
portance to field
ecology and evolutionary biology, is almost unexplored. It m
ay be opera- tionally difficult o
r even impossible on som
e types of organisms, but I believe
it is in fact feasible for many different types of anim
als in many different
environments.
This approach has great potential to m
easure the importance of selection
on traits in natural populations in natural environments. It also can be used
in situations in which the environm
ent has been experimentally altered. In
this case, the response of the trait in the population can be compared to
a priori
expectations about the effect of
such alteration. F
or instance, one m
ight remove predators and determ
ine whether burst speed o
r endurance declines in a population in the absence of this particular selective agent. O
ne m
ight supplement anim
als living in saline ponds or deserts w
ith fresh water
and investigate whether osm
otic tolerance or fluid-concentrating capacity
changes as a result of altered environmental circum
stances. An
excellent exam
ple of this experimental approach is provided by the study of F
erguson and F
ox (1984). A com
bination of studies, examining responses of popula-
tions in both natural and experimentally m
anipulated environments, has a
great deal of potential to help us understand the im
portance of various phys- iological processes to
total fitness of organisms. T
his approach presents a protocol for testing assum
ptions about adaptation, not simply asserting them
axiom
atically. I believe this is one of the most exciting new
developments
and directions for physiological ecology as a field.
De
term
ina
tion
of heritabilities o
f organismal o
r physiological characters F
or adaptation and evolution of a trait to occur, it m
ust have a genetic basis. W
ithout a heritable basis, selection on a trait within each generation w
ill not influence the variability o
r distribution of the trait in ensuing ger,erations. It is necessary, for exam
ple, for fast parents to have fast offspring if the popu-
lation is to respond to
a new agent that selects against slow
er individuals. S
tudies of the heritnbility of physiologicnl traits are n valunble supplement to
ecological studies because they permit the determ
ination of both the poten- tial of the trait to
evolve and the rapidity with w
hich the response can occur. S
ome progress has been m
ade in particular systems in identifying effects
of individual loci on organism
al physiology and perform
ance (e.g., Watt,
1977, 1983; DiM
ichele and Pow
ers, 1982; Chappell and S
nyder, 1984; Barnes
and Laurie-A
hlberg, 1986; Chapters 5 and 8). W
hile individual loci may have
identifiable effects, many of the traits of interest to
a physiological ecologist w
ill be under multilocus control. C
onsequently, the techniques of quantita- tive genetics w
ill be the most appropriate for exam
ining the inheritance of these characters (see F
alconer, 1981, and Chapter 9 for a general discussion
of the field and appropriate methodology). T
echniques involve examining the
similarities of traits in parents and offspring an
dlo
r among the offspring of
given parents. They require that the organism
s in question can be bred suc-
cessfully in the laboratory or that gravid fem
ales can be obtained that will
deliver offspring in the laboratory. Few
studies have examined the heritability of physiological
or perfor-
mance characters. M
ost of them have dealt w
ith the inheritance of locomo-
tor performance. Significant heritabilities have been found for speed in race
horses (Langlois, 1980; T
olley, Notter, and M
arlowe, 1983), speed in hum
ans (B
ouchard and Malina, 1983a, 1983b), burst speed and stam
ina in lizards (van B
erkum and T
suji, in press; R. B
. Huey, unpublished data) and snakes (S. J.
ArnoId and A
. F. Bennett, unpublished data; T
. Garland, unpublished data).
Defensive behaviors in snakes are also heritable (A
rnold and Bennett, 1984).
In these locomotor studies, a m
inimum
of 30 to 5
0%
of the variability among
individuals is genetic. Other types of
physiological traits have also been
found to be heritable: for exam
ple, growth rate and efficiency in pigs (Sm
ith, K
ing, and Gilbert, 1962), reproductive output of chickens (E
msley, D
icker- son, and K
ashyap, 1977), and thermoregulatory behaviors of m
ice (Lacy and
Lynch, 1979). O
bservations are so few at this point that a case m
ay be made
for a general investigation of t.he topic of heritability per se of physiological system
s in different types of animals. Future studies m
ay concentrate on more
specific genetic issues concerning this inheritance, but, given the multilocus
nature of these traits, these are bound to be m
ore difficult.
Conclusions
Interindividual physiological variability is rarely studied. How
ever, this vari- ation is real and repeatable in m
any physiological traits. I believe that the analysis of the causes and consequences of interindividual variability has m
ajor promise as an analytical tool in physiological studies. E
cological and com
parative physiology have often been characterized as major branches of
organismal biology, but their view
of the organism has been ideal o
r typo- logical. It has been that of the nonexistent anim
al that possesses the average value of all physiological, m
orphological, and behavioral attributes of the population. Such anim
als do
not exist. Real individuals are unique com
bi- nations of traits, som
e above and some below
average. It is time to
recognize the uniqueness of the individual and to
turn it to our advantage as biologists.
The analysis of variation can be useful in studies on physiological corre-
lation and mechanism
, on the importance of the variable to
fitness under natural conditions, and on the potential for inheritance of the trait, w
ith the consequent possibility of its adaptation and evolution. I d
o not suggest that
the study of variation should supplant other approaches nor that it is even feasible for all physiological variables. B
ut where such study is applicable, it
can be a powerful analytical tool, for analysis of both m
echanism and adap-
tation. Its particular advantage is that it can pull together so many different
aspects of biology, not only physiology and ecology, but also behavior, mor-
phology, population biology, and evolution. Biologists often treat these as
different areas, but of course individual organisms d
o not m
ake these arbi- trary divisions and distinctions. T
hey react to problem
s and opportunities as integrated organism
s. Appreciating and studying individual differences can
be a synthetic approach that puts the individual organism back into organ-
ismal biology and gives us a m
uch broader understanding of animals and
their evolution.
Ap
pen
dix
Th
e problem of m
ass-dependent correlation is so ubiquitous in correlation analysis that I w
ill provide an illustrative example of the utility of the analysis
of residuals. In Figure 7.3a, two physiological traits are found to be positively
associated when one is plotted as a function of the other. T
hese might, for
example, be length of a M
alphigian tubule and secretion rate in an insect, or tidal volum
e and anatomical dead space during ventilation in a m
amm
al. S
uch a result might lead one to conclude that the traits are positjvely linked
functionally. If, however, both traits are plotted as a function of body m
ass (F
igures 7.3b and 7.3
4 each is also found to
be strongly and positively mass
dependent. Are the traits truly linked to each other o
r is their apparent asso- ciation due to
their mutual but independent relationship to
body mass? T
his size influence m
ay be removed by exam
ining the deviation of each data point from
the mass regression line (i.e., the residuals of the regression). If these
mass-corrected residuals are then plotted against each other (F
igure 7.3d), their relationship can be exam
ined without the interfering effects of body
size. In the case illustrated, the traits are found to be negatively related to
each other, which is exactly the opposite of the original conclusion based on
Figure 7.3a. T
heir apparent positive association was due only to
their mutual
correlation with body m
ass. This w
as, of course, a contrived example: the
residuals might also have been positively associated o
r not significantly cor- related w
ith each other. Th
e point is that an examination of the original,
uncorrected data in Figure 7.3a w
ould not have permitted this assessm
ent.
Ackn
ow
ledg
men
ts 1
I thank S. J. Arnold, M
. E. Feder, T. G
arland, R. B. H
uey, G. V
. Lauder, H
. B. Shaffer, and C
. R. T
aylor for helpful discussions andlor comm
ents on the manuscript. Support
for the workshop w
as provided by NSF G
rant BSR 86-07794. Support for the author's research cited herein is from
NSF G
rants BSR 86-00066, DC
B 85-02218, D
EB
81- 14656, and P
CM
81-02331.
- 16
0 '
260 '
3b0 4
b0
40
TRA
IT 2 M
ASS
Fi GU
RE
7.3 A hypothetical exam
ple of the effect of mass-correlated
effects on
the apparent association between tw
o traits. Data are
reported for two traits and body m
ass in arbitrary units for ten individ- uals (A
through J) along with least-squares regression lines. (a) T
he two
traits are positively and significantly correlated when they are related
to each other directly. (b) and (c) Each trait is positively m
ass-corre- lated. (d) M
ass effects are removed by calculating residuals, that is, the
difference between the observed value for each individual and the
value predicted by the m
ass regression. These are plotted against each
other, demonstrating a significant negative association betw
een the
traits after the confounding effects of m
ass are eliminated. N
ote that opposite conclusions about th
e relationship between the traits w
ould b
e derived from (a) and (d).
References
Arnold, S. J. (1981) B
ehavioral variation in natural populations. I. Phenotypic, genetic and environm
ental correlations between chem
oreceptive responses to prey in the garter snake, T
hamnophis elegans. E
volution 35489-509. A
rnold, 5. J. (1983) Morphology, perform
ance and fitness. Am
. Zool. 23:347-361.
Arnold, 5. J., and B
ennett, A. F. (1984) B
ehavioural variation in natura1 populations. 111. A
ntipredator displays in the garter snake Tham
nophis radix. Anim
. Behav.
32:llO8-lll8.
Arnold, 5. J., and B
ennett, A. F. (in press) B
ehavioural variation in natural popula- tions. V
. Morphological correlates of locom
otion in the garter snake Tham
no- phis radix. B
iol. 1. Linn. Soc.
Barnes, P. T
., and Laurie-A
hlberg, C. C
. (1986) Genetic variability of flight m
etabo- lism
in Drosophila rnelanogaster. 111. E
ffects of Gpdh allozym
es and environ- m
ental temperature on pow
er output. Genetics 112:267-294.
Bennett, A
. F. (1980) The therm
al dependence of lizard behaviour. Anim
. Behav.
28:752-762. B
erman, S. L., C
ibischino, M., D
ellaripa, P., and Montren, L. (1985) Intraspecific
variation in the hindlimb m
usculature of the house sparrow. A
m. Z
ool. 25:21A.
Bouchard, C
., and Malina, R. M
. (1983a) Genetics for the sport scientist: selected
methodological considerations. E
xerc. Sport Sci. R
ev. 11:274-305. B
ouchard, C., and M
alina, R. M
. (1983b) Genetics of physiological fitness and
motor perform
ance. Exerc. S
port Sci. Rev. 11:306-339.
Calder, W
. A., 111. (1984) Size, F
unction, and Life H
istory. Cam
bridge, Mass.: H
ar- vard U
niversity Press. C
happell, M. A
., and Snyder, L. R. G
. (1984) Biochem
ical and physiological corre- lates of deer m
ouse a-chain hemoglobin polym
orphisms. Proc. N
atl. Acad. Sci.
U.S.A
. 815484-5488.
Christian, K
. A., T
racy, C. R
., and Porter, W
. P. (1985) Inter-individual and intra- individual variation in body tem
peratures of the Galapagos land iguana (C
ono- lophus pallidus). 1. T
herm. B
iol. 10:47-50. C
lose, R. (1964) Dynam
ic properties of fast and slow skeletal m
uscles of the rat dur- ing developm
ent.]. Physiol. (L
ond.) 173:74-95 C
lose, R. (1965) T
he relation between intrinsic speed of shortening and duration of
:he active state of m
uscle. 1. Physiol. (Lond.) 180542-559.
Crow
ley, S. R. (1985) Insensitivity to desiccation of sprint running perform
ance in the lizard S
celoporus undulatus.]. H
erpetol. 19:171-174. C
rowley, S. R
., and Pietruszka, R. D
. (1983) Aggressiveness and vocalization in the
leopard lizard (Gam
belia wislizennii [sic]): the influence of tem
perature. Anim
. B
ehav. 31:1055-1060. D
iMichele, L., and Pow
ers, D. A
. (1982) Physiological basis for swim
ming endur-
ance differences between L
DH
-B genotypes of F
undulus heteroclitus. Science 216:1014-1016.
Else, P. L., and B
ennett, A. F. (1987) T
he thermal dependence of locom
otor perfor- m
ance and muscle contractile function in the salam
ander Am
bystoma
tigrinum nebulosum
.]. E
xp. Biol., 128:219-233.
Em
sley, A., D
ickerson, G. E., and K
ashyap, T. S. (1977) G
enetic parameters in prog-
eny-test selection for field performance of strain-cross layers. Poult. Sci.
56:121-146. E
ndler, J. (1986) Natural Selection in the W
ild. Princeton, N
.J.: Princeton U
niversity Press.
Falconer, D. S. (1981) introduction to
Quantitative G
enetics, 2nd ed. New
York:
Longm
an. Felsenstein, J. (1985) Phylogenies and the com
parative method. A
m. N
atur. 125:l- 15.
Ferguson, G. W
., and Fox, S. F. (1984) Annual variation of survival advantage of
large juvenile side-blotched lizards, Uta stansburiana: its causes and evolution-
ary significance. Evolution 38:342-349.
Garland, T
., Jr. (1984) Physiological correlates of locomotory perform
ance in a liz- ard: an allom
erric approach. Am
.]. Physiol. 247:R
806-R815.
Garland, T
., Jr. (1985) Ontogenetic and individual variarion in size, shape and speed
in rhe Australian agam
id lizard Am
phibolurus nuchalis. 1. Zool. (L
ond.) 207:425-440.
Garland, T
., Jr., and Arnold, S. J. (1983) E
ffects of a full stomach on locom
otory perform
ance of juvenile garrer snakes (Tham
nophis elegans). Copeia
1983:1092-1096. G
ould, S. J., and Lew
ontin, R. C
. (1979) The spandrels of San M
arco and rhe Pan- glossian paradigm
: a critique of the adaptationist programm
e. Proc. R. Soc.
Lond. [B] 205581-598.
Hanken, J. (1983) H
igh incidence of limb skeletal varianrs in a peripheral popula-
tion of the red-backed salamander, Plethodon cinereus (A
mphibia: Plethodonri-
dae), from N
ova Scoria. Can. 1. 2001. 61:1925-1931.
Huey, R
. B., and B
ennett, A. F. (1986) A
comparative approach to
field and labora- tory studies in evolutionary ecology. In P
redator-Prey R
elationships: Perspec- tives an
d A
pproaches from the S
tudy of Low
er Vertebrates, ed. M
. E. Feder and G
. V. L
auder, pp. 82-98. Chicago: U
niversity of Chicago Press.
Huey, R
. B., and H
ertz, P. E. (1984) Is a jack-of-all-temperatures a m
aster of none? E
volution 38:441-444. John-A
lder, H. B. (1984) Seasonal variations in activity, aerobic energetic capacities,
and plasma thyroid horm
ones (T, and T
,) in an iguanid lizard.]. C
omp. Phys-
iol. 154:409-419. K
rebs, H. A
. (1975) The A
ugust Krogh Principle: "For m
any problems there is an
animal on w
hich it can be mosr conveniently studied."].
Exp. Z
ool. 194:221- 226.
Krogh, A
. (1929) Progress of physiology. Am
. 1. Physiol. 90:243-251. Lacy, F. C
., and Lynch, C
. B. (1979) Quantitative genetic analysis of tem
perature regularion in M
trs musculus. I. Partirioning of variance. G
enetics 91:743-753. Lande, R
., and Arnold, S. J. (1983) T
he measurem
enr of selection on correlared characters. E
volution 37:1210-1226. L
anglois, B. (1980) Heritability of racing ability in thoroughbreds-A
review
. Live-
stock Prod. Sci. 7591- 605.
Laurie-A
hlberg, C. C
., Maroni, G
., Bew
ley, G. C
., Lucchesi, J. C
., and Weir, B. S.
(1980) Quantitative genetic variarion of enzym
e activities in natural populations of D
rosophila rnelanogaster. Proc. Natl. A
cad. Sci. U.S.A
. 77:1073-1077. M
ayr, E. (1982) The G
rowth of B
iological Thought: D
iversity, Evolution, and
Inheritance. Cam
bridge, Mass.: B
elknap. Pough, F. H
., and Andrew
s, R. M
. (1984) Individual and sibling-group variation in m
etabolism of lizards: the aerobic capacity m
odel for the evolution of endo- therm
y. Com
p. Biochem
. Physiol. 79A:415-419.
Putnam, R
. W., and B
ennett, A. F. (1981) T
hermal dependence of behavioural per-
formance of anuran am
phibians. Anim
. Behav. 29502-509.
Ringler, N
. H. (1983) V
ariation in foraging ractics in fishes. In Predators and Prey
in Fishes, ed. D. L. G
. Noakes, D
. G. L
indquist, G. S. H
elfman, and J. A
. Ward,
pp. 159-171. The H
ague: Dr. W
. Junk.
Schmidt-N
ielsen, K. (1984) Scaling: W
hy Is Anim
al Size So Im
portant? Cam
bridge U
niversity Press. Shaffer, H
. B., and Lauder, G
. V. (1985a) Patterns of variation in aquatic am
bysto- m
atid salamanders: kinem
atics of the feeding mechanism
. Evolution 39:83-92.
Shaffer, H. B
., and Lauder, G
. V. (1985b) A
quatic prey capture in ambystom
atid sal- am
anders: patterns of variation in muscle activity.].
Morphol. 183:273-284.
Simpson, G
. G. (1953) T
he Major Features of E
uolution. New
York: C
olumbia U
ni- versity Press.
Smith, D
., King, J. W
. B., and Gilbert, N
. (1962) Genetic param
eters of British L
arge W
hite pigs. Anim
. Prod. 4:128-143. Sullivan, B. K., and W
alsberg, G. E. (1985) C
all rate and aerobic capacity in Wood-
house's toad (Bufo w
oodhousei). Herpetologica 41:404-407.
Taigen, T
. L., and Wells, K
. D. (1985) E
nergetics of vocalization by an anuran am
phibian (Hyla versicolor). 1. C
omp. Ph ysiol. 155:163-170.
Tolley, E. A., N
otter, D. R
., and Marlow
e, T. J. (1983) H
eritability and repeatability of speed for tw
o-and three-year-old standard bred racehorses. 1. Anim
. Sci. 56:1294-1305.
Toolson, E. C
. (19841 Interindividual variation in epicuticular hydrocarbon composi-
tion and water loss rates of the cicada, T
ibicen dealbatus (Hom
optera: Cicadi-
dae). Physiol. Zool. 57:550-556.
van Berkum
, F. H., and T
suji, J. S. (in press) Am
ong-family differences inisprint
speed of hatchling Sceloporus occidentalis. 1. Zool. (L
ond.) W
att, W. B. (1977) A
daptation at specific loci. 1. Natural selection on phosphoglu-
cose isomerase in C
olias butterflies: biochemical and population aspects. G
enet- ics 87:177-194.
Watt, W
. B. (1983) Adaptation at specific loci. 11. D
emographic and biochem
ical ele- m
ents in the maintenance of the C
olias PGI polym
orphism. G
enetics 103:691- 724.
Wells, D
. K., and T
aigen, T. L. (1984) R
eproductive behavior and aerobic capacities of m
ale Am
erican toads (Bufo am
ericanus): is behavior constrained by physiol- ogy? H
erpetologica 40:292-298.
Discussion
LIN
DS
TE
DT
: I agree w
ith B
ennett that there are identifiable
individuals w
hich are low perform
ers - they have a lo
w m
axim
um
oxygen consumption,
a low m
axim
um
running speed, etc. - and there are oth
er individuals that are high perform
ers. But o
n any given day a low
-performing anim
al may
outperform th
e high-performing anim
als: the ranges of their perform
ances overlap, even if their m
eans are repeatedly different. Th
e likelihood of find-
ing mechanistic differences to
account for those mean differences m
ay be rather low
. We
still need to have th
e broader overview betw
een species,
wh
ere we have a higher signal-to-noise ratio.
BE
NN
ET
T: I a
m n
ot advocating th
at we abandon all o
ther approaches for
the study of variation, n
or th
at we should ignore th
e means. B
ut we
should
take interindividual variations into account in addition. Sometim
es the least and m
ost able individuals overlap, but you can still find that the individual differences are statistically repeatable.
LIN
DS
TE
DT
: Y
es, we do try to do that. By the sam
e token, I think we have
to be cautious about throwing out sim
pler statistics because they are simple,
especially if we risk losing som
e biological insight w
ith greater statistical sophistication. For exam
ple, in using stepwise m
ultiple regression, it can be hard to intuit w
hat the result means. A
lso, we have found that as w
e increase the sam
ple size, the total proportion of explained variation changes very lit- tle, yet the relative contributions of various independent variables to
the total explained variation changes a great deal. A
gain, that leads me to
gain less insight.
BENNETT: I agree that m
any times the sim
ple statistics are adequate, but w
here they are inadequate, we should not continue using the old m
odels and old w
ays of doing things. Th
e stepwise m
ultiple regression approach seems
to me to be a tool to
suggest further directions for study. If you find that no
factors are correlated w
ith performance (m
easured as burst speeds), that may
tell you that you should be looking at other factors. When you do have sig-
nificant correlations, then you have a basis for further experimental analysis.
It is a first pass in looking for important variables.
SCH
EID: I agree that interindividual variability is really im
portant. Nature
intends to tell us something that w
e have mostly neglected so far. N
ow, is it
not true that if you want to
address the interindividual variability, then you have to look at the intraindividual variability first? In fact, the only thing that rem
ains beyond intraindividual variability is true interindividual variability.
BENNETT: T
hat's right. You have to be able to m
ake repeated measures on
individuals. This is feasible for som
e factors and unfeasible for other factors. If you are looking at w
hole-body lactate content, for instance, you can do
that only once. B
ut there are a large number of physiological characters, such
as blood flow param
eters, that we can now
sample nondestructively because
of improved instrum
entation.
SCHEID: W
e now have im
proved techniques to w
ork on
uninstrumented,
nonanesthetized animals, w
hich is mandatory if you w
ant to ask questions
about variability. I think that the techniques were not form
erly available to
address this variability in a meaningful w
ay.
I HU
EY: T
he standard statistical m
ethod of m
easuring repeatability is the
intraclass correlation coefficient, which m
easures the proportion of the vari- ation that is due to
difference among individuals versus w
ithin individuals. By that
measure, som
etimes the types of
measurem
ents that Bennett w
as
referring to are highly repeatable: m
ost of the variation is among individuals
and not within individuals. F
or example, A
rt Dunham
and I looked at sprint speeds of lizards in natural populations over a w
hole year, and the repeat- abilities are on the order of 0.5 to 0.6, w
hich is higher than in thoroughbred horses.
That is probably
high enough that w
e, can begin to analyze the
mechanistic basis of individual variation and also look at the adaptive sig-
nificance of that variation.
PO
WE
RS
: O
ne problem of reproducing the sam
e experiment on the sam
e individual is that som
e organisms becom
e trained. In addition, we found that
we cannot put m
ore than one individual in a track at a time because of behav-
ioral interactions between them
.
BE
NN
ET
T: For running speed, in about half of the species that w
e observe, w
e see what w
e assume is a conditioning effect, from
day one to day tw
o, but after that the m
eans stay exactly the same, the order of the individuals
stays the same. S
ome species show
this initial effect, others don't.
PO
WE
RS
: One thing we have to
do
with fish is to
acclimate them
to w
ater that is m
oving at a constant speed, for thirty to sixty days. Everything from
then on is very reproducible. I am
sure that a lot of the variation in the lit- erature is a function of this training phenom
enon and where the organism
s cam
e from.
FL
OR
AN
T:
I think that developmental effects can be extrem
ely important,
and I wondered w
hether you were rearing these anim
als in the lab or being
careful about the developmental processes that w
ere going on prior to, dur- ing, and after birth.
BE
NN
ET
T: All the anim
als that we have been dealing w
ith are adult animals,
taken directly from the field and tested w
ithin a matter of days. In the breed-
ing studies, gravid animals are collected and young anim
als are born under constant conditions in the laboratory. T
he whole issue of developm
ental effects and constancy of rank-ordered perform
ance over time has not even
begun to be explored.
FU
TU
YM
A:
Suppose you are interested in very short term
acclimation effects,
the capacity of the individual
to change its phenotype from
m
oment to
mom
ent, which is the opposite of repeatability. H
ow
do
you deal with that?
There are interesting questions there as w
ell.
BE
NN
ET
T: Y
OU
begin by im
mediately asking questions about your equip-
ment and techniques, and get that out of the w
ay first. Then perhaps you can
begin building correlations from m
oment to m
oment by m
easuring the vari- ables sequentially, to
see whether you are getting tracking of one variable by
the other.
INT
ER
IND
IVID
UA
L V
AR
IAB
ILIT
Y
169
AR
NO
LD
: W
e can examine the capacity to
change performance over short
or long periods of time as traits, and that's a virtually unexplored area. B
ut it is not th
e opposite of repeatability. Suppose w
e define a new variable that
represents the capacity to change perform
ance as a function of an elevation in tem
perature from 10 OC
to 20 O
C. We can m
easure its repeatability, we
can ask whether it is inherited, w
hether it is genetically correlated with other
traits, and so forth. The statistical field for dealing w
ith such traits is some-
times called profile analysis of variance.
FE
DE
R: I w
ant to shift the focus of this discussion to
the point that Bennett
made about the prospect for perform
ing natural experiments using natural
populations. I am very excited about this prospect. U
sing the variation in populations as a substrate, altering an environm
ental variable for individuals in a population or adding individuals to a population and looking at the effects could potentially be a very pow
erful technique. Dennis P
owers said
that it may soon be possible to take individual genes and m
ove them into or
out of individual organisms, w
hich could offer us a lot of insight.
PO
WE
RS
: It is already possible for som
e species. In lower vertebrates,.it w
ill probably take another year.
DA
WS
ON
: T
here are detraining or conditioning effects that go with captiv-
ity. When w
e studied cold resistance in small birds, w
e found that the ani- m
als maintained in outdoor flight cages, given the seeds of the type that they
were using naturally, abandoned their w
inter fattening, perhaps because they had assured m
eals and more com
plicated cues. They also had m
uch lower
cold resistance than freshly captured animals. If
one is dealing with badly
distorted responses, which is som
etimes a risk w
ith wild anim
als, that ought to be determ
ined. A good deal of w
hat one may be dealing w
ith in animals
long standing in captivity may not be relevant to
the natural situation.
FLOR
AN
T: In keeping hibernators for many years in the lab, the hibernators
begin to free-run, and it is as if certain physiological responses occur at "non-
adaptive" times of year. T
his obscures the optimal tim
e that the animal per-
forms a particular response under natural circum
stances.
BENN
ETT: These are valid concerns. O
ne way of keeping track of them
is to run appropriate controls, so that w
e can place boundaries on the magni-
tude of the captivity responses.
DA
WS
ON
: By attem
pting to determ
ine repeatability,
if you
start early enough, -you can discern if there are any effects of that type. T
hat is not done a lot. T
his is a caveat about use of material from
animal dealers, w
hich may
have a very fuzzy history indeed.
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